Non-native plant drives the spatial dynamics of its herbivores: the
case of black locust (Robinia pseudoacacia) in EuropeNon-native
plant drives the spatial dynamics of its herbivores: the case of
black locust
(Robinia pseudoacacia) in Europe
Richard Mally1, Samuel F. Ward2, Jií Trombik1, Jaroslaw Buszko3,
Vladimir Medzihorsky1, Andrew M. Liebhold1,4
1 Czech University of Life Sciences, Faculty of Forestry and
Wood Sciences, Kamýcká 129, 165 00 Prague 6 – Suchdol, Czech
Republic 2 Mississippi State University, Department of
Biochemistry, Molecular Biology, Entomology and Plant Pathology,
Mississippi State, MS 39762, USA 3 Nicolaus Copernicus
University, Toru, Poland 4 USDA Forest Service Northern
Research Station, 180 Canfield St., Morgantown, WV 26505, USA
Corresponding author: Richard Mally (
[email protected])
Academic editor: Jianghua Sun | Received 22
July 2021 | Accepted 30 September
2021 | Published 9 November 2021
Citation: Mally R, Ward SF, Trombik J, Buszko J, Medzihorsky V,
Liebhold AM (2021) Non-native plant drives the spatial dynamics of
its herbivores: the case of black locust (Robinia pseudoacacia) in
Europe. NeoBiota 69: 155–175.
https://doi.org/10.3897/neobiota.69.71949
Abstract Non-native plants typically benefit from enemy release
following their naturalization in non-native habi- tats. However,
over time, herbivorous insects specializing on such plants may
invade from the native range and thereby diminish the benefits of
enemy release that these plants may experience. In this study, we
compare rates of invasion spread across Europe of three North
American insect folivores: the Lepidop- tera leaf miners
Macrosaccus robiniella and Parectopa robiniella, and the gall midge
Obolodiplosis robiniae, that specialize on Robinia pseudoacacia.
This tree species is one of the most widespread non-native trees in
Europe. We find that spread rates vary among the three species and
that some of this variation can be explained by differences in
their life history traits. We also report that geographical
variation in spread rates are influenced by distribution of Robinia
pseudoacacia, human population and temperature, though Robinia
pseudoacacia occurrence had the greatest influence. The importance
of host tree occurrence on invasion speed can be explained by the
general importance of hosts on the population growth and spread of
invading species.
Keywords Black locust, Diptera, Lepidoptera, Macrosaccus
robiniella, Obolodiplosis robiniae, Parectopa robiniella, Robinia
pseudoacacia
NeoBiota 69: 155–175 (2021)
doi: 10.3897/neobiota.69.71949
https://neobiota.pensoft.net
Copyright Richard Mally et al. This is an open access article
distributed under the terms of the Creative Commons Attribution
License (CC BY 4.0), which permits unrestricted use, distribution,
and reproduction in any medium, provided the original author and
source are credited.
RESEARCH ARTICLE
A peer-reviewed open-access journal
Introduction
Plants introduced to new, non-native habitats may have an advantage
over the native flora by escaping herbivore pressure, allowing them
to allocate more resources toward vegetative and reproductive
growth, as formulated e.g. in the enemy release hypothesis (Keane
and Crawley 2002). In such a setting, non-native plants can quickly
become widespread and invade various habitats. Black locust,
Robinia pseudoacacia (Fabaceae), is a prime example of this, now
being one of the most widespread non-native trees in Europe
(Vítková et al. 2016). The native range of this species is limited
to the central Appalachian and Ouachita mountains and the Ozark
Plateau in the Eastern and Central United States (Huntley 1990).
Black locust was introduced to Europe during the first half of the
17th century as an ornamental tree planted in parks and gardens
(Wein 1930), and from 1750 on, it was used in forest plantations in
Central Europe for purposes of timber and honey production. From
these plantings, it spread prolifically and is cur- rently found
throughout most of temperate and sub-Mediterranean Europe
(Fig. 1A), displacing native vegetation and altering ecosystem
properties (Vítková et al. 2016).
Although widely distributed, European populations of black locust
were little af- fected by the few native generalist herbivores
feeding on it, with generally marginal impact on the tree (e.g.
Bartha et al. 2008). In contrast, five specialist herbivores ac-
cidentally introduced to Europe from the native range of black
locust were found to have a considerably higher impact on the tree.
The first North American insect species discovered feeding on
Robinia in Europe was the sawfly Euura tibialis (Newman, 1837)
(Hymenoptera: Tenthredinidae), formerly placed in Nematus (Prous et
al. 2014). This species was first recorded in Europe in 1825
(Rasplus et al. 2010), twelve years before the species’ formal
description from the Isle of Wight (Newman 1837). In Europe, this
parthenogenetic species is found feeding on Robinia pseudoacacia
and R. viscosa, while in its original North American range it also
feeds on R. hispida and Gleditsia triacanthos (Darling and Smith
1985; Liston 2011).
More recently, four additional Robinia herbivores were accidentally
introduced from North America to Europe: In 1970, Parectopa
robiniella Clemens, 1863, a Lepi- doptera leaf miner of the
Gracillariidae family, was recorded from Northern Italy (Vidano and
Marletto 1972). It was followed by Appendiseta robiniae (Gillette,
1907) (Aphididae), an aphid first found in 1978 in Italy (Micieli
De Biase and Calambuca 1979). Another Gracillariidae leaf miner,
Macrosaccus robiniella (Clemens, 1859), was first found in 1983 in
Northern Switzerland (Whitebread 1990). This species was placed in
Phyllonorycter Hübner, 1822 until recently, when it was transferred
to Mac- rosaccus Davis & De Prins, 2011 (Davis and De Prins
2011). Finally, in 2003 the black locust gall midge, Obolodiplosis
robiniae (Haldeman, 1847) (Diptera: Cecidomyiidae), was reported
from Northeast Italy (Duso and Skuhravá 2002). Upon the arrival of
the four most recently introduced Robinia herbivores in Europe,
black locust was widely distributed and naturalized on the
continent. The four herbivore species thus found their food source
in abundance and were subject to little competition from more gen-
eralist native European herbivores, so that they could extend their
distribution range.
Spread of Robinia pseudoacacia herbivores in Europe 157
Relatively little is known about how the range expansion of
specialized non-native herbivorous insects is affected by the
distribution of their native host plant in non- native regions.
European Robinia pseudoacacia and its introduced specialist
herbivores are a prime opportunity to study such a setting in more
detail. In order to better un- derstand the factors promoting the
range expansion of these non-native herbivores and to better
predict spread patterns in other parts of black locust’s non-native
range, we analyze the three most well-documented Robinia herbivores
present in Europe (P. ro- biniella, M. robiniella, and O.
robiniae), their patterns of historical spread across the
continent, and potential factors facilitating this spread. For
this, we investigate and quantify different potential drivers of
the spread of these herbivores: Robinia distribu- tion, human
population, mean annual temperature and precipitation, and proxim-
ity to previously invaded regions. We hypothesize that both the
human population and R. pseudoacacia distribution would
positively affect herbivore spread via effects on propagule
pressure and habitat invasibility.
Methods
In order to avoid confusion among the similar species names, we
will refer to the three species by their genus names, i.e.,
Parectopa for P. robiniella, Macrosaccus for M. rob- iniella, and
Obolodiplosis for O. robiniae. In figures and tables, we state the
full species names. We furthermore refer to Robinia pseudoacacia
simply as Robinia, unless other Robinia species are
mentioned.
Country and regional first records of the presence of Parectopa,
Macrosaccus and Obolodiplosis across Europe were obtained from the
published literature, online data- bases and in one case from a
photographic record. Coordinates for the localities were obtained
through Wikipedia’s GeoHack
(https://www.mediawiki.org/wiki/GeoHack) and Google Maps
(https://www.google.com/maps). Suppl. material 1: Table S1 pro-
vides a full list of records for the three folivore species. We
also obtained georeferenced occurrence records for each of these
three species at a global scale. These were sourced from GBIF
(https://www.gbif.org), EPPO (https://gd.eppo.int), CABI
(https://www. cabi.org/ISC), Davis and De Prins (2011) and Shang et
al. (2015). These global re- cords were not used for analysis of
spread rates.
Radial rates of spread were estimated for each species from
European first re- cords using the distance regression method
(Gilbert and Liebhold 2010). Accord- ing to this method, a linear
regression model was fit to the distance from the first discovery
point in Europe as a function of year of first discovery. The slope
of the estimated regression equation provides an estimate of the
radial rate of range expan- sion. Distances between the
distribution records were calculated with the R packages geosphere
1.5-10 (Hijmans et al. 2019) and sp 1.4-2 (Pebesma and Bivand 2005;
Bivand et al. 2013), using the ’Vincenty’ (ellipsoid) great circle
distance function (distVincentyEllipsoid). Linear regressions were
performed using the lm function in the R language.
Richard Mally et al. / NeoBiota 69: 155–175 (2021)158
In order to explore factors affecting spread of each species, we
applied Cox Propor- tional Hazard analysis following the approach
used by Ward et al. (2020). This model quantifies the probability
that each uninvaded location will become invaded at annual time
steps as a function of a series of candidate explanatory variables.
Five predictors for herbivore spread were considered: human
population, Robinia distribution, mean an- nual precipitation, mean
annual temperature (see Fig. 1), and spatial proximity. Human
population (expressed as number of inhabitants in the year 2000)
was extracted from a human population density raster at a
resolution of 30 arc-seconds from the Global Ru- ral-Urban Mapping
Project (Balk et al. 2006). Data on Robinia distribution (expressed
as total tree area in km2) were extracted from the European Atlas
of Forest Tree Species (Sitzia et al. 2016) as a relative
probability of presence raster at a resolution of 1 km, based on
the C-SMFA model and field observations (de Rigo et al. 2016).
Values of total annual precipitation (cm) and annual mean
temperature (°C) for the period 1970–2000 were obtained from the
WorldClim v2 database (Fick and Hijmans 2017) at a resolu- tion of
30 arc-seconds. No data on Robinia distribution were available for
points located in Moldova, Belarus, Ukraine and the European part
of Russia. Values for each variable were calculated for areas in a
10 or 50 km buffer radius zones around each of the indi- vidual
records for each species. Spatial proximity (sp) to previously
invaded points (asso- ciated with diffusive propagule pressure) was
a time-varying predictor and calculated as:
1
=∑ ,
where d is the distance (in km) between a given point i and each
previously invaded point j. Thus, spatial proximity was estimated
for each point in each year, while all other predictors did not
change annually. Human population and Robinia distribution were
log-transformed to reduce skewness.
In addition to locations of individual records for each species,
the Cox proportional hazard model was fit using “pseudo-absence”
points. These are locations falling outside of the invaded range of
each species that were never invaded during the time span of
records. Pseudo-absence records were generated in a 50 km grid
across a 300 km buffer zone outside of the minimum convex hulls
around each set of records for each species (see Fig. 2). The
minimum convex hull, individual buffer zones and spatial statistics
for the selected variables were created using ESRI ArcMap 10.5.1
(ESRI 2016).
Given uncertainty about the identity of most relevant spatial
scales of the predictor variables, all possible combinations of 10
km and 50 km scale predictors were fit in full models. The model
with the lowest Akaike Information Criterion (AIC; Akaike 1973) was
then further reduced (if applicable) by iteratively removing
predictors with the higher p-value until all remaining were p <
0.05. To assess robustness of our models to the missing values of
Robinia density for Eastern Europe, the entire model fitting and
selection process was redone without considering Robinia
distribution as a predictor. Models were fit using the R package
survival 3.2-7 (Therneau 2020).
Spread of Robinia pseudoacacia herbivores in Europe 159
Results
We assembled 97 first record locations from 24 countries for
Parectopa, 92 locations from 25 countries for Macrosaccus, and 75
locations from 33 countries for Obolodiplosis (Fig. 2; Suppl.
material 1: Table S1; Mally et al. 2021). Linear regressions show a
highly sig- nificant correlation between time and distance from the
invasion focus for all three her- bivores: the radial rate of
spread estimated by linear regression (Fig. 3) is 35.4 ±
5.7 km/ year (t95 = 6.16, p < 0.005) for Parectopa, 73.42 ±
5.0 km/year (t90 = 14.79, p < 0.005) for Macrosaccus, and 128.3
± 8.1 km/year (t73 = 15.79, p < 0.005) for Obolodiplosis.
Macrosaccus mainly spread east- and northward in the first two
decades after its in- troduction (Fig. 2B), as did Parectopa. The
latter species was first discovered in North- ern Italy, south of
the Alps. In order to reach the areas north of the Alps, it spread
east- and later northward around this mountain range that acted as
a geographical barrier (Fig. 2A). Obolodiplosis spread more or less
equally in all directions from its first occurrence location in
Northern Italy. Within Europe, it is the most widespread of the
three investigated Robinia herbivores, with distribution records
stretching from Portugal to the Caspian Sea and from Sicily to
Southern Sweden and the Baltic states
Figure 1. Variables investigated for their influence on the spread
of the three Robinia-specific herbivores in Europe A estimated
distribution of Robinia pseudoacacia B human population C mean
annual precipi- tation D mean annual temperature.
Richard Mally et al. / NeoBiota 69: 155–175 (2021)160
(Fig. 2C). In the 18 years since its first discovery in Europe, it
has invaded a larger area than either of the two leaf miners, which
had been introduced considerably earlier.
Results of the reduced Cox proportional hazard models are shown in
Table 2, cor- relation matrices of predictors for the best-fitting
model for the three species in Suppl. material 2: Tables S4–S6, and
Akaike Information Criterion (AIC) values for the three species in
Suppl. material 2: Tables S7–S9. Annual mean precipitation is found
to have the least predictive power among the five investigated
predictors. It is absent in all re- duced models (Table 2), and is
significant only for Parectopa in the full model (Suppl. material
2: Table S2). In the reduced (Table 2) and full (Suppl. material 2:
Table S2) models, colder annual mean temperatures were associated
with an increased risk of invasion for Parectopa and Macrosaccus
(as indicated by the negative Z-scores), and less so for
Obolodiplosis. In the models with Robinia omitted (Suppl. material
2: Table S3), it is significant for Parectopa, and less so for
Macrosaccus; no significance is observed for Obolodiplosis. In the
full and the reduced models, human population has a highly sig-
nificant positive influence on the invasion risk for Parectopa and
Macrosaccus, and less so for Obolodiplosis. In the models with
Robinia omitted (Suppl. material 2: Table S3), it is highly
significant for all three species. Robinia distribution is found to
be the most
Figure 2. European records for A Parectopa robiniella B Macrosaccus
robiniella, and C Obolodiplosis rob- iniae. The first European
record for each species is marked by a star, the subsequent spread
is indicated by color-coded records in 5-year (A, B) or 2-year (C)
intervals. The grid of black points around the distribu- tion areas
marks pseudo-absence locations in a 300 km buffer region formed by
the minimum convex hull around the records for each species.
Spread of Robinia pseudoacacia herbivores in Europe 161
Table 1. Results of the linear regression of distance over time for
the three herbivore species. Radial rate of spread (km per year) is
provided by the slope of the regression.
Intercept ± SE Slope (radial rate of spread) ± SE Multiple
R-squared Parectopa robiniella -10.06 ± 201.60 35.37 ± 5.7 0.29
Macrosaccus robiniella -354.72 ± 107.55 73.42 ± 5.0 0.71
Obolodiplosis robiniae 270.69 ± 84.08 128.29 ± 8.12 0.77
Table 2. Results of reduced Cox proportional hazards (CPH) models
with lowest AIC and all predictors with p < 0.05.
Species Predictor Coefficient SE Z p Parectopa robiniella spatial
proximity sp 3.67 0.80 4.59 <0.0001
human population (50 km) 0.61 0.09 6.61 <0.0001 Robinia (10 km)
0.59 0.07 7.89 <0.0001
temperature (50 km) -0.61 0.08 -8.10 <0.0001 precipitation (10
km) -0.0032 0.0011 -2.98 0.0029
Macrosaccus robiniella spatial proximity sp 22.87 2.61 8.78
<0.0001 human population (10 km) 0.58 0.08 7.64 <0.0001
Robinia (50 km) 0.40 0.06 6.76 <0.0001 temperature (50 km) -0.58
0.09 -6.37 <0.0001
Obolodiplosis robiniae spatial proximity sp 40.08 15.74 2.55 0.0109
human population (10 km) 0.37 0.11 3.35 0.0008
Robinia (50 km) 0.44 0.06 7.05 < 0.0001 temperature (50 km)
-0.13 0.06 -2.07 0.0382
Figure 3. Linear regression scatterplots of distance (in km) from
first record in Europe over time, for A Parectopa robiniella B
Macrosaccus robiniella, and C Obolodiplosis robiniae.
Richard Mally et al. / NeoBiota 69: 155–175 (2021)162
consistent predictor, explaining the spread of all three species
with high significance both in the full and the reduced models. In
the full and the reduced models, proxim- ity to previously invaded
areas is highly significant for Parectopa and Macrosaccus, but much
less so for Obolodiplosis. In the models without Robinia, it is
highly significant for all three species, along with human
population.
The known global distribution of Robinia is shown in Fig. 4A, and
the distribu- tions of the three herbivore species are shown in
Fig. 4B–D. Robinia is widely distrib- uted in virtually every
temperate and subtropical portion of the world. The distribu- tions
of the three herbivore species appear to be more limited. Of the
three species, Obolodiplosis is the most widely distributed, having
established in Europe, East Asia and New Zealand. However, there is
no record of its presence in either the Afrotropic or Neotropic
regions. The two Lepidoptera species Parectopa and Macrosaccus
appear to be slightly less successful invaders, having only
established in Europe.
Discussion
The three herbivores show similar patterns of radial range
expansion in Europe, al- though with substantially different annual
spread rates. All three species were initially discovered in the
same general region of south-central Europe with only
~200–400 km separating their sites of initial discovery.
Strikingly, Parectopa, which was the first of the three
investigated Robinia herbivores to be recorded from Europe over 50
years ago, has the smallest annual spread rate (about 35 km/year)
and is reported from the fewest number of countries (24).
Macrosaccus, first reported 13 years later in 1983, exhibits an
average spread rate of 73 km/year, but spread much faster in
Hungary with
Figure 4. Global distribution of A Robinia pseudoacacia B Parectopa
robiniella C Macrosaccus robiniella and D Obolodiplosis robiniae
compiled from our own dataset, GBIF, EPPO, CABI, Davis and De Prins
(2011) and Shang et al. (2015).
Spread of Robinia pseudoacacia herbivores in Europe 163
its abundant black locust stands, invading the entire country from
west to east in two years (Csóka 2001). The species is currently
recorded from 25 European countries. The newest invader,
Obolodiplosis, has the by far highest spread rate (128 km/year) and
has spread to 33 countries since its first report in 2003. Of the
three species, Obolodiplosis has also spread the most widely on the
global scale (Fig. 4D). While Obolodiplosis has successfully
invaded Europe, East Asia and New Zealand, Parectopa and
Macrosaccus have only invaded Europe. In North America, all three
species have also extended their range beyond the native range of
Robinia, with Macrosaccus and Obolodiplosis having spread as far as
the west coast of the US and Canada.
Invasion spread is driven by population growth coupled with
movement. Thus, any factors that affect either population growth or
movement are likely to influence patterns of spread. It is likely
that the differences in invasion patterns observed among these
species (both within Europe and globally) can be attributed to
their biological traits that influence their population growth
rates or dispersal, either natural disper- sal or accidental
long-distance movement by humans. Obolodiplosis develops through
three generations per year in the Czech Republic, and in up to four
generations in more southern regions such as Italy, Hungary and
Serbia (Skuhravá et al. 2007; Mihajlovi et al. 2008; Duso et al.
2011). For China, however, up to six generations per year have been
reported (Shang et al. 2015). The capacity for this species to
develop through multiple generations likely facilitates rapid
population growth (Fahrner and Aukema 2018). The small size of
adults also probably leads to this species being easily trans-
ported in wind though such natural dispersal probably only
facilitates local dispersal. Long-distance transport (including
inter-continental spread) is most likely to occur via hitch-hiking
with cargo, vehicles, etc. Pupation of Obolodiplosis takes place in
the galls, except for the last generation of a year, where pupation
takes place in the soil (Uechi et al. 2005; Tóth et al. 2009).
Because this species overwinters as a diapausing larva (Duso et al.
2011), this probably creates potential for the species to be
accidentally transported long distances with vehicles and other
objects that might be placed under Robinia trees prior to
transport.
Even though both of the two leaf miner species belong to the same
Lepidoptera family (Gracillariidae), their biologies exhibit
differences that potentially explain dif- ferences observed in
their success and rate of spreading across Europe. Parectopa pro-
duces two to three generations per year, with two in more northern
regions such as Belarus, and up to three in more southern regions
like Transnistria (Moldova) and Croatia (Maceljski and Igrc 1984;
Antyukhova 2010; Sautkin and Evdoshenko 2012). Macrosaccus is
reported to produce two to five generations per year: two
generations in Southern Germany, Switzerland and Austria (Wipking
1991; Huemer et al. 1992; Huemer 1993; Rietschel 1996), two to
three generations in Hungary (Csóka 2001), three generations in
Serbia and Belarus (Stojanovi and Markovi 2005; Sautkin and
Evdoshenko 2012), four generations in Slovenia (Seljak 1995), and
potentially even a fifth generation in Croatia (Maceljski and Meši
2001). Furthermore, often two to three (and up to eight)
Macrosaccus larvae share a common mine (Huemer 1993; Rietschel
1996; Šefrová 2001), whereas Parectopa caterpillars usually
inhabit
Richard Mally et al. / NeoBiota 69: 155–175 (2021)164
mines solitarily (Baugnée 2014). In addition to a generally higher
reproduction rate, Macrosaccus may thus be able to attain a higher
population density.
Pupation takes place in the leaf litter in the case of Parectopa,
whereas Macrosaccus larvae pupate on the leaves (Antyukhova 2010;
Davis and De Prins 2011). In urban areas, Parectopa pupae might
therefore be removed with the leaf litter in the autumn (Antyukhova
2010), whereas Macrosaccus, which overwinters in the adult stage
(De- schka 1995), probably remains on or near its host plants,
increasing its chances of re- occupying Robinia stands in the
following season. However, pupating in the leaf litter, where it is
presumably less exposed to parasitoids, might increase the survival
of Parec- topa as compared to Macrosaccus (Csóka et al. 2009).
Given that Parectopa exhibits the slowest rate of spread of all
three species, we can hypothesize that their biology of
overwintering as pupae in leaf litter does not facilitate their
anthropogenic movement to the extent seen in Macrosaccus and
Obolodiplosis.
The small adult body size and wing anatomy of the two leaf miners
indicate that they likely spread passively with wind, but transport
of hibernating or resting adults with trade cannot be excluded
(Rietschel 1996; Šefrová 2001, 2003). Passive wind transportation
might explain the generally stronger eastward spread of the leaf
miners with the prevailing west winds in Central Europe.
We find a negative correlation between mean annual temperature and
the spread of the two leaf miners, meaning that colder temperatures
promote the spread of these species. Considering the geographical
setting in which the range expansion of these species occurred,
this is not surprising: with their first records in Northern Italy
resp. Northern Switzerland, range expansion would occur mostly
north- and eastward, as expansion southwards is limited by the
Mediterranean Sea. The nega- tive correlation between temperature
and spread might thus be a result of generally more sampling points
in the north- and eastward direction of the points of first record,
where annual mean temperatures are generally lower than those in
Northern Italy (see Fig. 1D).
Our findings of colder annual mean temperatures promoting the
spread of both leaf miners are in contrast to published information
at least of Parectopa, which is re- ported to be “more
thermophilous” than Macrosaccus (Baugnée 2014). This is consist-
ent with its slower northward spread and its presence in Southern
Italy (i.e., south of the Emilia Romagna region), where Macrosaccus
is absent (Stoch 2003). Parectopa was also reported as “massively
present” with 50–80% of leaflets infested in the hot and dry, sandy
environments of coastal Croatia, whereas habitats in inland Croatia
with a more continental climate experienced a low infestation rate
of 3% (Maceljski and Igrc 1984; Stojanovi and Markovi 2005).
Parectopa thus seems to have more specialized habitat requirements
than Macrosaccus. Parectopa might therefore continue its spread in
the more southern parts of Europe and into the Transcaucasian
region where its hostplant is present. Fodor and Hârua (2009) find
almost no niche overlap between Parectopa and Macrosaccus in
Romania, despite both utilizing Robinia leaves as their food
source, where they occupy mostly opposite sides and different parts
of the leaflets. The two leaf miners are thus not in direct
competition for their food source.
Spread of Robinia pseudoacacia herbivores in Europe 165
Both leaf miner species are often reported to exhibit high
population densities dur- ing their initial colonization phase
following establishment in a new region, while sub- sequently
becoming much rarer (Seljak 1995; Šefrová 2001; Tomov 2003;
Antyukhova 2010; Baugnée 2014). In Poland however, Parectopa was
mostly first recorded from single mines in isolated locations,
apparently as a result of anemochorous dispersal. The following
absence of Parectopa mines in these locations for several years
suggests that these founder populations were unable to establish.
More successful northward spread of Parectopa occurred along river
valleys, e.g. the Vistula valley, where Robinia finds favorable
growing conditions on the sunny slopes (JB, pers. obs.).
Macrosaccus, on the other hand, quickly spread through Poland over
a wide front and in consider- able abundance until 2005, when areas
of rarer Robinia occurrence (presumably due to less suitable growth
conditions) were reached (JB, pers. obs.). There are also records
of Obolodiplosis being very abundant in recently invaded regions,
particularly in East Asia (Yang et al. 2006). Though lacking
quantitative data, it appears that none of the three species is
particularly abundant in their native range in North America (AML,
pers. obs.). Along these lines, we note that most of the records of
Obolodiplosis from North America lie outside of the native range of
its host, Robinia, which may be indicative of the low abundance of
Obolodiplosis in its native range.
Parasitization might play an important role in the speed of spread.
Since their establishment in Europe, the two leaf miners have
accumulated a large number of generalist parasitoids (summarized in
Serini 1990; De Prins and De Prins 2006–2020, and Csóka et al.
2009), with 20 species recorded for Parectopa, and 37 for
Macrosaccus. Parasitization rates vary considerably though, ranging
in the case of Macrosaccus from 1–3% in Upper Austria (Deschka
1995), 10–30% in Southern Moravia (Šefrová 2001), <40% in
Kraków, Poland (Wojciechowicz-ytko and Jankowska 2004), 35–50% in
Trentino, Italy (Angeli et al. 1996), up to 47.6% in Hungary (Csóka
et al. 2009), and >60% in Bosnia-Herzegovina (Dimi et al. 2000),
to 30–67.5% in Serbia (Stojanovi and Markovi 2005). Information on
parasitization rates in Parectopa are few, reach- ing a maximum of
15.3% in Hungary, where Macrosaccus is up to three times more
heavily parasitized (Csóka et al. 2009). Obolodiplosis hosts few
parasitoids, which likely promotes its rapid spread in Europe and
other regions of the world. It is to be expected that Obolodiplosis
will have a fairly large impact on Robinia populations wherever it
is introduced, which might however be compensated by the fast
growth and reproductive abilities of Robinia. On the other hand,
Platygaster robiniae, the gall midge’s primary parasitoid infesting
the host eggs and feeding gregariously on the larvae (Buhl and Duso
2008; Duso et al. 2011; Kim et al. 2011), is reported to cause
parasitization rates of 51.6% to 84.8% (Park et al. 2009; Lu et al.
2010), making it a promising candidate as control agent of the
locust gall midge (Lu et al. 2010).
Our quantitative analysis indicates local Robinia density to be the
single factor having the strongest impact on the spread of
Parectopa, Macrosaccus and Obolodiplosis across Europe. Skuhravá et
al. (2007) reached a similar conclusion for Obolodiplosis based on
a qualitative evaluation of historical European spread. Since
feeding of all three insect species is limited to Robinia, it is
understandable that its density would
Richard Mally et al. / NeoBiota 69: 155–175 (2021)166
strongly affect population growth rates and consequently affect
spread. Several other studies have reported that host densities
influence rates of invasion spread of invading species (e.g., Meier
et al. 2014; Hudgins et al. 2017; Ward et al. 2020). The resource
concentration hypothesis posits that more abundant host plant
resources promote in- sect herbivore population growth rates
(Hambäck and Englund 2005), and such el- evated rates can be
expected to translate into increased invasion spread rates.
The fact that Robinia is itself an invasive species has interesting
implications re- garding the positive effect of Robinia density on
spread of these folivore species. It has been noted that at a
global scale, plant invasions or widespread planting of non-native
plants promote invasions by herbivore species that use these plants
as hosts (Liebhold et al. 2018; Branco et al. 2019; Guo et al.
2019). There are many examples in which abundant distributions of
non-native plants have promoted invasions by insect herbi- vores
that specialize on those plants (e.g., Hurley et al. 2016). This
phenomenon can be regarded as a type of “invasion meltdown” where
invasion by one species triggers subsequent invasions of other
species (Simberloff and Von Holle 1999). However, less is known
about how host insect invasions can mediate invasions of their
parasites be- yond theoretical studies (e.g., Fagan et al.
2002).
Previous studies have also identified human population density to
be related to the spread of invading insect species (Gilbert et al.
2004; Ward et al. 2020). It is logi- cal that humans may
accidentally transport insect life stages and therefore promote
long-distance dispersal. Population models show that when
occasional long-distance dispersal is coupled with frequent
short-distance dispersal, this leads to much greater rates of
spread than when long-distance spread is lacking (Shigesada et al.
1995; Hastings et al. 2005). Long-distance dispersal is often
associated with passive move- ment by humans and thus high human
densities may drive higher rates of long- distance movement and
thereby facilitate invasion spread (Gippet et al. 2019). But the
significant influence of human population may also be confounded
with Robinia occurrence since human-caused disturbance typically
promotes this tree species (Vít- ková et al. 2016).
Similar to human population, annual mean temperature was found to
have a sig- nificant influence on the spread of the two leaf
miners, but less so for the gall midge. This result is in
concordance with the wider climate spectrum of invaded regions of
Obolodiplosis: in Europe, the gall midge is now distributed from
the hot-summer Med- iterranean climate of Portugal, Sicily and
Greece to the humid continental climate of Southern Sweden and the
Baltic states. On the global scale, it has been recorded from
Vancouver Island, Canada (Skuhravá et al. 2007), Japan and South
Korea (Kodoi et al. 2003; Woo et al. 2003; Uechi et al. 2005;
Tokuda et al. 2019), China (Yang et al. 2006; Shang et al. 2015),
the Russian Far East (Csóka et al. 2017), and New Zealand
(Anonymous 2009; Bain 2009) (Fig. 4D). Parectopa and Macrosaccus,
on the other hand, have only been reported outside their native
range from Europe and the west coast of North America (Fig. 4B, C).
In contrast to mean temperature, we found an- nual mean
precipitation to have no significant influence on the spread of the
three herbivore species.
Spread of Robinia pseudoacacia herbivores in Europe 167
Our results indicate that spatial proximity to previously invaded
regions plays an important role for the spread of Parectopa and
Macrosaccus, but much less so for the gall midge Obolodiplosis.
Obolodiplosis showed an extremely fast spread across most of Europe
in the 18 years since its first record in Europe, now occupying a
considerably larger area than the much earlier established leaf
miners. The results of Roques et al. (2016) indicate that it spread
faster than any other insect species invading Europe in their
analysis. The spread of this species exhibited several long-
distance jumps to form discontinuous populations, the most
prominent one being a 2,000 km dispersal from its first record in
Northeast Italy to the East Ukraine in just three years.
Furthermore, Obolodiplosis successfully invaded the islands of
Great Britain, Sicily, Corfu, and the Balearic Islands, none of
which have been reached by either of the two leaf miners. Skuhravá
et al. (2007) speculate that the gall midge may frequently be
transported over long distances with nursery trees, and/or through
passive transport by freight traffic. Our finding that spatial
proximity to previously invaded areas plays a minor role in the
spread of Obolodiplosis concord with its high spread rate of 128.3
km/year, and the observed long-distance dispersal.
None of the scatterplots of the three herbivore species (Fig. 3)
show a clear es- tablishment phase preceding the expansion phase.
Macrosaccus, however, was closely monitored in the area of its
first discovery in 1983 around Basel in Northern Switzer- land.
There, the distribution range did not exceed an 85 km radius around
Basel by 1989, although the species was “already common around
Basle in 1983” (Whitebread 1990). The absence of a clear
establishment phase in the scatterplots might indicate that the
species arrived some years before their first record in Europe,
when they had time to establish a sufficiently large population and
propagule pressure to expand their ranges. The scatterplots also
provide little evidence of geographical “saturation” in any of
these three species. As invading species spread to all suitable
areas in a region, such plots can be expected to asymptotically
stop increasing (Shigesada and Kawasaki 1997). Eventually, all
three species can be anticipated to become established in all re-
gions with suitable habitat. That environmental niche is presumably
defined both by the presence of a suitable climate and by the
presence of Robinia hosts. Comparison of the current distribution
of these species (Fig. 2) with the distribution of Robinia suggests
that all three species will soon saturate their potential habitat.
However, on a global scale these same species are far from
saturation and further invasions can be anticipated in the
future.
In addition to these three species that utilize Robinia as a host,
Hargrove (1986) identified 72 other herbivore species associated
with Robinia in its native North American range. Given the three
species studied here, along with Euura tibialis and Appendiseta
robiniae, it is evident that only five out of 75 North American
Robinia specialists have presently invaded Europe. Thus, we can
anticipate that additional herbivore species are likely to invade
Europe and elsewhere in Robinia’s invaded range and that this will
contribute to the dilution of enemy release in populations of this
invasive plant.
Richard Mally et al. / NeoBiota 69: 155–175 (2021)168
Conclusion
Specialist herbivores are crucially dependent on the presence of
their host plant. Our results show that the widespread presence of
Robinia in Europe, especially in human- influenced environments,
greatly facilitated the spread of the introduced North Ameri- can
herbivores. The excessive proliferation of Robinia increases the
likelihood of estab- lishment and spread of non-native specialist
herbivores, thus creating a negative feed- back where the initial
beneficial effects of enemy release on Robinia are diminished, and
Robinia populations are potentially reduced.
With Robinia having been introduced to most regions of the world
with a suit- able temperate climate, conditions are thus beneficial
for the establishment of these insects, and potentially other
specialist herbivores from black locust’s native range.
Obolodiplosis has already become established in East Asia and New
Zealand, where it has exhibited rapid spread similar to that in
Europe. Its success can be attributed to the ability for
long-distance jumps as well as to life history traits, such as high
reproduction rates, and a presumably small guild of parasitoids.
For the two leaf miner species, spa- tial proximity to previously
invaded areas is another important factor affecting range
expansion, reflecting the ability of these species to disperse into
adjacent uninvaded areas following initial colonization. Although
the three investigated herbivores invaded Europe under similar
conditions, there are pronounced differences in their invasion
success, which can be explained with species-specific life history
traits. Furthermore, pan-European cargo traffic has increased over
the past decades, increasing the likeli- hood of long-distance
spreading.
Acknowledgements
We are grateful to Lenka Pešková (ZU library), Josep Ylla (Gurb
(Barcelona), Spain), Elisenda Olivella (Natural Sciences Museum of
Barcelona, Spain), Ivan Bacherikov (Saint Petersburg State Forest
Technical University, Russia), Jan Havlíek (Karolinum Press,
Charles University Prague, Czech Republic), Valentyna Meshkova
(Ukrainian Research Institute of Forestry and Forest Melioration,
Kharkiv, Ukraine) and Hana Šefrová (Mendel University Brno, Czech
Republic) for help with literature search and acquisition. Nico
Schneider (Ministère de l’Education nationale, Luxembourg), Erik
van Nieukerken (Naturalis Leiden, the Netherlands), Vladimir Krpach
(State Univer- sity of Tetova, North Macedonia), Charles Eiseman
(Northfield, Massachusetts, USA) and Francesca Vegliante (Museum
für Tierkunde Dresden, Germany) helped with in- formation on
distribution records.
This research was supported by the grant “Advanced research
supporting the forestry and woodprocessing sector’s adaptation to
global change and the 4th industrial revolu- tion,” No.
CZ.02.1.01/0.0/0.0/16_019/0000803 financed by OP RDE, as well as by
the IGA A_21_21 project of the Czech University of Life Sciences
internal grant agency.
The authors declare that there is no conflict of interest regarding
the publication of this paper.
Spread of Robinia pseudoacacia herbivores in Europe 169
References
Akaike H (1973) Information theory and an extension of the maximum
likelihood principle. In: Petrov BN, Csáki F (Eds) 2nd
International Symposium on Information Theory, Tsahkad- sor,
Armenia, USSR, September 2–8, 1971, Budapest: Akadémiai Kiadó,
267–281.
Angeli G, Apollonio N, Forti D (1996) Behaviour of leaf miner
Phyllonorycter robiniellus (Lepi- doptera Gracillariidae) in
Trentino surroundings and possibility of control. Informatore
Fitopatologico 10: 50–54.
Anonymous (2009) Pest watch: 1 April 2009 – 22 May 2009.
Biosecurity 92(June): 33–35. Antyukhova OV (2010) Beloakatzievaya
mol-pestrianka (Parectopa robiniella Clemens) – opas-
nii vreditel Robinia pseudoacacia L. v Pridnestrovie [White acacia
moth (Parectopa robin- iella Clemens) – a dangerous pest of Robinia
pseudoacacia L. in the Transnistria]. Izvestiya Sankt-Peterburgskoi
Gosudarstvennoi Lesotekhnicheskoi Akademii 192: 4–11.
Bain J (2009) New insect on Robinia, Obolodiplosis robiniae. In:
Farm Forestry New Zealand.
https://www.nzffa.org.nz/farm-forestry-model/the-essentials/forest-health-pests-and-dis-
eases/Pests/obolodiplosis-robiniae-robinia-gall-midge/new-insect-on-robinia/
Balk DL, Deichmann U, Yetman G, Pozzi F, Hay SI, Nelson A (2006)
Determining global population distribution: Methods, applications
and data. Advances in Parasitology 62: 119–156.
https://doi.org/10.1016/S0065-308X(05)62004-0
Bartha D, Csiszár Á, Zsigmond V (2008) Black locust (Robinia
pseudoacacia L.). In: Botta- Dukát Z, Balogh L (Eds) The most
important invasive plants in Hungary. Institute of Ecology and
Botany, Hungarian Academy of Sciences, Vácrátót, Hungary,
63–76.
Baugnée J-Y (2014) Parectopa robiniella (Lepidoptera:
Gracillariidae), a leafminer of black lo- cust Robinia
pseudoacacia, new to the Belgian fauna. Phegea 42: 55–57.
http://www.phe- gea.org/Phegea/2014/Phegea42-3_55-57.pdf
Bivand RS, Pebesema E, Gomez-Rubio V (2013) Applied spatial data
analysis with R, 2nd edn. Springer, NY, [xviii +] 405 pp.
https://doi.org/10.1007/978-1-4614-7618-4
Branco M, Nunes P, Roques A, Fernandes MR, Orazio C, Jactel H
(2019) Urban trees fa- cilitate the establishment of non-native
forest insects. NeoBiota 52: 25–46. https://doi.
org/10.3897/neobiota.52.36358
Buhl PN, Duso C (2008) Platygaster robiniae n. sp. (Hymenoptera:
Platygastridae) Parasitoid of Obolodiplosis robiniae (Diptera:
Cecidomyiidae) in Europe. Annals of the Entomological So- ciety of
America 101(2): 297–300.
https://doi.org/10.1603/0013-8746(2008)101[297:PR
NSHP]2.0.CO;2
Csóka G (2001) Recent invasions of five species of leafmining
Lepidoptera in Hungary. In: Lieb- hold AM, McManus ML, Otvos IS,
Fosbroke SLC (Eds) Proceedings „Integrated Manage- ment of Forest
Defoliating Insects”. USDA General Technical Reports NE-277:
31–36.
Csóka G, Pénzes Z, Hirka A, Mikó I, Matoševi D, George M (2009)
Parasitoid assemblages of two invading black locust leaf miners,
Phyllonorycter robiniella and Parectopa robiniella in Hungary.
Periodicum Biologorum 111(4): 405–411.
https://hrcak.srce.hr/47878
Csóka G, Stone GN, Melika G (2017) Non-native gall-inducing insects
on forest trees: a global review. Biological Invasions 19:
3161–3181. https://doi.org/10.1007/s10530-017-1466-5
Darling DC, Smith DR (1985) Description and life history of a new
species of Nematus (Hy- menoptera: Tenthredinidae) on Robinia
hispida (Fabaceae) in New York. Proceedings of the
Entomological Society of Washington 87(1): 225–230.
https://www.biodiversitylibrary.
org/item/54866#page/233/mode/1up
Davis DR, De Prins J (2011) Systematics and biology of the new
genus Macrosaccus with de- scriptions of two new species
(Lepidoptera, Gracillariidae). ZooKeys 98: 29–82. https://
doi.org/10.3897/zookeys.98.925
De Prins, J, De Prins W (2006–2020) Global taxonomic database of
Gracillariidae (Lepidop- tera). World Wide Web electronic
publication. http://www.gracillariidae.net [date of acces- sion
2021/05/03] https://doi.org/10.1163/9789004475397
de Rigo D, Caudullo G, Houston Durrant T, San-Miguel-Ayanz J (2016)
The European Atlas of Forest Tree Species: modelling, data and
information on forest tree species. In: San-Miguel- Ayanz J, de
Rigo D, Caudullo G, Houston Durrant T, Mauri A (Eds) European Atlas
of Forest Tree Species. Publ. Off. EU, Luxembourg, 40–45.
https://ies-ows.jrc.ec.europa.eu/
efdac/download/Atlas/pdf/Modelling_data_and_information_on_forest_tree_species.pdf
Deschka G (1995) Schmetterlinge als Einwanderer. Stapfia 37:
77–128. Dimi N, Dautbaši M, Magud B (2000) Phyllonorycter
robiniella Clemens, a new leaf miner
species in the entomofauna of Bosnia-Herzegovina. Works of the
Faculty of Forestry, Uni- versity of Sarajevo 1: 7–15.
Duso C, Skuhravá M (2002) First record of Obolodiplosis robiniae
(Haldeman) (Diptera Cecid- omyiidae) galling leaves of Robinia
pseudacacia L. (Fabaceae) in Italy and Europe. Frustula
Entomologica 25: 117–122.
Duso C, Boaria A, Surian L, Buhl PN (2011) Seasonal abundance of
the Nearctic gall midge Obolodiplosis robiniae in Italy and the
impact of its antagonist Platygaster robiniae on pest populations.
Annals of the Entomological Society of America 104(2): 180–191.
https:// doi.org/10.1603/AN10030
ESRI (2016) ArcGIS j ArcMap 10.5 (10.5.1). Redlands, CA:
Environmental Systems Research Institute.
https://www.arcgis.com/features/index.html
Fagan WF, Lewis MA, Neubert MG, Van Den Driessche P (2002) Invasion
theory and biological control. Ecology Letters 5(1): 148–157.
https://doi.org/10.1046/j.1461-0248.2002.0_285.x
Fahrner S, Aukema BH (2018) Correlates of spread rates for
introduced insects. Global Ecol- ogy and Biogeography 27: 734–743.
https://doi.org/10.1111/geb.12737
Fick SE, Hijmans RJ (2017) WorldClim 2: new 1km spatial resolution
climate surfaces for global land areas. International Journal of
Climatology 37: 4302–4315. https://doi. org/10.1002/joc.5086
Fodor E, Hârua O (2009) Niche partition of two invasive insect
species, Parectopa robiniella (Lepidoptera; Gracillariidae) and
Phyllonorycter robiniella (Clem.) (Lepidoptera: Gracillari- idae).
Research Journal of Agricultural Science 41(2): 261–269.
http://rjas.ro/download/
paper_version.paper_file.8c94429aea2cc457.3336362e706466.pdf
Gilbert M, Liebhold A (2010) Comparing methods for measuring the
rate of spread of invading populations. Ecography 33(5): 809–817.
https://doi.org/10.1111/j.1600-0587.2009.06018.x
Gilbert M, Grégoire J-C, Freise JF, Heitland W (2004) Long-distance
dispersal and human population density allow the prediction of
invasive patterns in the horse chestnut leafminer Cameraria
ohridella. Journal of Animal Ecology 73: 459–468.
https://doi.org/10.1111/ j.0021-8790.2004.00820.x
Gippet JM, Liebhold AM, Fenn-Moltu G, Bertelsmeier C (2019)
Human-mediated disper- sal in insects. Current Opinion in Insect
Science 35: 96–102. https://doi.org/10.1016/j.
cois.2019.07.005
Guo Q, Fei S, Potter KM, Liebhold AM, Wen J (2019) Tree diversity
regulates forest pest inva- sion. Proceedings of the National
Academy of Sciences 116(15): 7382–7386. https://doi.
org/10.1073/pnas.1821039116
Hambäck PA, Englund G (2005) Patch area, population density and the
scaling of migration rates: the resource concentration hypothesis
revisited. Ecology Letters 8(10): 1057–1065.
https://doi.org/10.1111/j.1461-0248.2005.00811.x
Hargrove WW (1986) An annotated species list of insect herbivores
commonly associated with black locust, Robinia pseudoacacia, in the
Southern Appalachians. Entomological News 97(1): 36–40.
https://www.biodiversitylibrary.org/page/2723423#page/290/mode/1up
Hastings A, Cuddington K, Davies KF, Dugaw CJ, Elmendorf S,
Freestone A, Harrison S, Holland M, Lambrinos J, Malvadkar U,
Melbourne BA (2005) The spatial spread of inva- sions: new
developments in theory and evidence. Ecology Letters 8(1): 91–101.
https:// doi.org/10.1111/j.1461-0248.2004.00687.x
Hijmans RJ, Williams E, Vennes C (2019) geosphere: Spherical
Trigonometry. https://cran.r- project.org/package=geosphere
Hudgins EJ, Liebhold AM, Leung B (2017) Predicting the spread of
all invasive forest pests in the United States. Ecology Letters
20(4): 426–435. https://doi.org/10.1111/ele.12741
Huemer P (1993) Zur Arealexpansion zweier schädlicher
Robinienminiermotten nach Öster- reich. Forstschutz aktuell 12/13:
11–12.
Huemer P, Deutsch H, Habeler H, Lichtenberger F (1992) Neue und
bemerkenswerte Funde von Kleinschmetterlingen in Österreich.
Berichte des Naturwissenschaftlich-medizinischen Vereins in
Innsbruck 79: 199–202.
https://www.zobodat.at/pdf/BERI_79_0199-0202.pdf
Huntley JC (1990) Robinia pseudoacacia L., Black Locust Leguminosae
Legume family. In: Silvics of North America 2, 755–761.
http://dendro.cnre.vt.edu/dendrology/USDAFSSilvics/40.pdf
Hurley BP, Garnas J, Wingfield MJ, Branco M, Richardson DM,
Slippers B (2016) Increasing numbers and intercontinental spread of
invasive insects on eucalypts. Biological Invasions 18: 921–933.
https://doi.org/10.1007/s10530-016-1081-x
Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy
release hypothesis. Trends in Ecology and Evolution 17: 164–170.
https://doi.org/10.1016/S0169-5347(02)02499-0
Kim, I-K, Park J-D, Shin S-C, Parek I-K (2011) Prolonged embryonic
stage and synchro- nized life-history of Platygaster robiniae
(Hymenoptera: Platygastridae), a parasitoid of Obolodiplosis
robiniae (Diptera: Cecidomyiidae). Biological Control 57(1): 24–30.
https:// doi.org/10.1016/j.biocontrol.2010.12.007
Kodoi F, Lee H-S, Uechi N, Yukawa J (2003) Occurrence of
Obolodiplosis robiniae (Diptera: Cecidomyiidae) in Japan and South
Korea. Esakia 43: 35–41.
Liebhold AM, Yamanaka T, Roques A, Augustin S, Chown SL,
Brockerhoff EG, Pyšek P (2018) Plant diversity drives global
patterns of insect invasions. Scientific Reports 8(1): 1–5.
https://doi.org/10.1038/s41598-018-30605-4
Liston AD (2011) New hostplant records for European sawflies
(Hymenoptera, Tenthredini- dae). Entomologist’s Monthly Magazine
146: 189–193.
Richard Mally et al. / NeoBiota 69: 155–175 (2021)172
Lu C-K, Buhl PN, Duso C, Zhao C-M, Zhang J-S, Ji Z-X, Gao S-H, Yu
J-Y, Wen X-L (2010) First discovery of Platygaster robiniae
(Hymenoptera: Platygastridae) parasitizing the inva- sive
Obolodiplosis robiniae (Diptera: Cecidomyiidae), a gall maker in
China. Acta Entomo- logica Sinica 53(2): 233–237.
Maceljski M, Igrc J (1984) Bagremov miner (Parectopa robiniella
Clemens (Lepidoptera, Gracil- laridae) u Jugoslaviji. Zaštita bilja
35(4): 323–331.
Maceljski M, Meši A (2001) Phyllonorycter robiniella Clemens a new
insect pest in Croa- tia. Agriculturae Conspectus Scientificus
66(4): 225–230. https://hrcak.srce.hr/index.
php?show=clanak_download&id_clanak_jezik=19256
Mally R, Ward S F, Trombik J, Buszko J, Medzihorský V, Liebhold A M
(2021) European oc- currence records of the Robinia herbivores
Parectopa robiniella, Macrosaccus robiniella and Obolodiplosis
robiniella compiled from literature records and personal
observations. Neo- Biota. https://doi.org/10.15468/qnrsen [accessed
via GBIF.org on 2021-10-22]
Meier CM, Bonte D, Kaitala A, Ovaskainen O (2014) Invasion rate of
deer ked depends on spatiotemporal variation in host density.
Bulletin of Entomological Research 104(3): 314–322.
https://doi.org/10.1017/S0007485314000042
Micieli De Biase L, Calambuca E (1979) L’Appendiseta robiniae
(Gillette), nuova specie per l’italia su Robinia pseudoacacia L.
Informatore Fitopatologico 11–12: 31–33.
Mihajlovi L, Glavendeki MM, Jakovljevi I, Marjanovi S (2008)
Obolodiplosis robiniae (Hal- deman) (Diptera: Cecidomyiidae) – a
new invasive insect pest on black locust in Serbia. Bulletin of the
Faculty of Forestry 97: 197–208.
https://doi.org/10.2298/GSF0897197M
Newman E (1837) Notes on Tenthredinina. The Entomological Magazine
4: 258–263. https://
www.biodiversitylibrary.org/item/35924#page/278/mode/1up
Park J-D, Shin S-C, Kim C-S, Jeon M-J, Park I-K (2009) Biological
characteristic of Obolodiplo- sis robiniae and control effects of
some insecticides. Korean Journal of Applied Entomology 48(3):
327–333. https://doi.org/10.5656/KSAE.2009.48.3.327
Pebesma EJ, Bivand RS (2005) Classes and methods for spatial data
in R. News, The Newsletter of the R Project 5: 9–13.
Prous M, Blank SM, Goulet H, Heibo E, Liston A, Malm T, Nyman T,
Schmidt S, Smith DR, Vårdal H, Viitasaari M, Vikberg V, Taeger A
(2014) The genera of Nematinae (Hy- menoptera, Tenthredinidae).
Journal of Hymenoptera Research 40: 1–69. https://doi.
org/10.3897/JHR.40.7442
Rasplus J-Y, Villemant C, Rosa Paiva M, Delvare G, Roques A (2010)
Hymenoptera. Chapter 12. In: Roques A, Kenis M, Lees D,
Lopez-Vaamonde C, Rabitsch W, Rasplus J-Y, Roy D (Eds) Al- ien
terrestrial arthropods of Europe. BioRisk 4: 669–776.
https://doi.org/10.3897/biorisk.4.55
Rietschel G (1996) Zum Auftreten von Phyllonorycter robiniella
(Clemens, 1859) (Lepidop- tera, Gracillariidae), einer Miniermotte
der Robinie, in Süddeutschland. Philippia 7(4): 315–318.
https://www.zobodat.at/pdf/Philippia_7_0315-0318.pdf
Roques A, Auger-Rozenberg M-A, Blackburn TM, Garnas J, Pyšek P,
Rabitsch W, Richardson DM, Wingfield MJ, Liebhold AM, Duncan RP
(2016) Temporal and interspecific varia- tion in rates of spread
for insect species invading Europe during the last 200 years.
Biologi- cal Invasions 18(4): 907–920.
https://doi.org/10.1007/s10530-016-1080-y
Sautkin F, Evdoshenko S (2012) Sovremenoe rasprostranenie v
usloviah Belarusii invazivnih vidov miniruiushih moley
(Lepidoptera: Gracillariidae) – fillofagov-minerov beloi
akatzii
(Robinia pseudoacacia) [Current distribution in Belarus of invasive
species of miner moths (Lepidoptera: Gracillariidae) –
phyllophagous miners of white acacia (Robinia pseudoaca- cia)].
Vestnik BGU 2(1): 103–104.
Šefrová H (2001) Phyllonorycter robiniella (Clemens, 1859) – egg,
larva, bionomics and its spread in Europe (Lepidoptera,
Gracillariidae). Acta Universitatis Agriculturae et Silvicul- turae
Mendelianae Brunensis 50(3): 7–12.
Šefrová H (2003) Invasions of Lithocolletinae species in Europe –
causes, kinds, limits and ecological impact (Lepidoptera,
Gracillariidae). Ekológia 22(2): 132–142.
Seljak G (1995) Phyllonorycter robiniella (Clemens), another new
Lithocolletida of the Robinia in Slovenia. Gozdarski Vestnik 53:
78–82.
Serini GB (1990) Parassioidi di Parectopa robiniella Clemens e di
Phyllonorycter robiniellus (Cle- mens) (Lepidoptera
Gracillariidae). Bollettino di zoologia agraria e di bachicoltura
22(2): 139–149.
Shang X, Yao Y, Huai W, Zhao W (2015) Population genetic
differentiation of the black locust gall midge Obolodiplosis
robiniae (Haldeman) (Diptera: Cecidomyiidae): a North Ameri- can
pest invading Asia. Bulletin of Entomological Research 105:
736–742. https://doi. org/10.1017/S000748531500070X
Shigesada N, Kawasaki K, Takeda Y (1995) Modeling stratified
diffusion in biological inva- sions. The American Naturalist
146(2): 229–251. https://doi.org/10.1086/285796
Simberloff D, Von Holle B (1999) Positive interactions of
nonindigenous species: invasional meltdown? Biological invasions
1(1): 21–32. https://doi.org/10.1023/A:1010086329619
Sitzia T, Cierjacks A, de Rigo D, Caudullo G (2016) Robinia
pseudoacacia in Europe distribu- tion, habitat, usage and threats.
In: San-Miguel-Ayanz J, de Rigo D, Caudullo G, Hou- ston Durrant T,
Mauri A (Eds) European Atlas of Forest Tree Species. Publ. Off. EU,
Luxembourg, 166–167.
https://ies-ows.jrc.ec.europa.eu/efdac/download/Atlas/pdf/Rob-
inia_pseudoacacia.pdf
Skuhravá M, Skuhravý V, Csóka G (2007) Invasive spread of the gall
midge Obolodiplosis rob- iniae in Europe. Cecidology 22:
84–90.
Stoch F (2003) Checklist of the species of the Italian fauna.
https://www.faunaitalia.it/check- list/introduction.html
Stojanovi A, Markovi (2005) Parasitoid complex of Phyllonorycter
robiniella (Clemens, 1859) (Lepidoptera, Gracillariidae) in Serbia.
Journal of Pest Science 78: 109–114. https://
doi.org/10.1007/s10340-004-0077-y
Therneau TM (2020) Survival Analysis [R package survival version
3.2-7]. https://cran.r-pro- ject.org/package=survival
Tokuda M, Uechi N, Yukawa J (2019) Invasive pest species of
gall-inducing Cecidomyiidae (Dip- tera) in Japan. Formosan
Entomology 38: 33–41. https://doi.org/10.6662/TESFE.2018017
Tomov RI (2003) Phyllonorycter robiniella (Clemens, 1859)
(Lepidoptera, Gracillariidae), new pest on Robinia pseudoacacia L.
in Bulgaria. Proceedings, scientific papers. The 50th anni- versary
of University of Forestry Sofia (2003): 105–107.
Tóth P, Váová M, Lukáš J (2009) The distribution of Obolodiplosis
robiniae on black locust in Slovakia. Journal of Pest Science 82:
61–66. https://doi.org/10.1007/s10340-008-0220-2
Uechi N, Yukawa J, Usuba S (2005) Recent distribution records of an
alien gall midge, Obolodiplosis robiniae (Diptera: Cecidomyiidae)
in Japan, and a brief description of its pu-
Vidano C, Marletto F (1972) Parectopa robiniella a new pest of
Robinia pseudacacia in Europe. In: Proceedings: International
Apicultural Congress, 23d, Moscow, 1971.
Vítková M, Müllerová J, Sádlo J, Pergl J, Pyšek P (2016) Black
locust (Robinia pseudoacacia) beloved and despised: A story of an
invasive tree in Central Europe. Forest Ecology and Management
384(2017): 287–302.
https://doi.org/10.1016/j.foreco.2016.10.057
Ward SF, Fei S, Liebhold AM (2020) Temporal dynamics and drivers of
landscapelevel spread by emerald ash borer. Journal of Applied
Ecology 57(6): 1020–1030. https://doi.
org/10.1111/1365-2664.13613
Wein K (1930) Die erste Einführung nordamerikanischer Gehölze in
Europa. Mitteilungen Deutsche Dendrologische Gesellschaft 42:
137–163.
Whitebread SE (1990) Phyllonorycter robiniella (Clemens, 1859) in
Europe (Lepidoptera, Gracillariidae). Nota Lepidopterologica 12:
344–353. https://www.biodiversitylibrary.org/
item/139985#page/360/mode/1up
Wojciechowicz-ytko E, Jankowska B (2004) The occurrence and
harmfulness of Phyllonorycter robiniella (Clem.), a new leafminer
of Robinia pseudoacacia L. trees. Electronic Journal of Polish
Agricultural Universities, Horticulture 7(1): [1–11].
http://www.ejpau.media.pl/
articles/volume7/issue1/horticulture/art-06.pdf
Woo K-S, Choe HJ, Kim H-J (2003) A report on the occurrence of
yellow locust midge Obolodiplosis robiniae (Haldeman, 1987) from
Korea. Korean Journal of Applied Ento- mology 42(1): 77–79.
Yang Z-Q, Qiao X-R, Bu W-X, Yao Y-X, Xiao Y, Han Y-S (2006) First
discovery of an impor- tant invasive insect pest, Obolodiplosis
robiniae (Diptera: Cecidomyiidae) in China. Acta Entomologica
Sinica 49: 1050–1053.
Supplementary material 1
Table S1. First record locations of Parectopa robiniella,
Macrosaccus robiniella and Obolodiplosis robiniae from Europe.
Authors: Richard Mally Data type: occurrences Explanation note: An
XLSX worksheet containing three tabs, one for each of the
three
investigated black locust herbivores Parectopa robiniella,
Macrosaccus robiniella and Obolodiplosis robiniae, with the first
locations (with country, administrative area, city and specific
locality, where available), longitude, latitude, observation year
and reference of the record.
Copyright notice: This dataset is made available under the Open
Database License (http://opendatacommons.org/licenses/odbl/1.0/).
The Open Database License (ODbL) is a license agreement intended to
allow users to freely share, modify, and use this Dataset while
maintaining this same freedom for others, provided that the
original source and author(s) are credited.
Link: https://doi.org/10.3897/neobiota.69.71949.suppl1
Supplementary material 2
Tables S2–S9 Authors: Richard Mally, Samuel F. Ward, Jií Trombik,
Jaroslaw Buszko, Vladimir Medzihorsky, Andrew M. Liebhold Data
type: docx. file Explanation note: Table S2. Results of full Cox
proportional hazards (CPH) models
for all predictors with p < 0.05. Table S3. Results of full Cox
proportional haz- ards (CPH) models with Robinia distribution
removed as predictor, with p < 0.05. Table S4. Correlation
matrix of predictors for best-fitting model for Parectopa ro-
biniella. Table S5. Correlation matrix of predictors for
best-fitting model for Mac- rosaccus robiniella. Table S6.
Correlation matrix of predictors for best-fitting model for
Obolodiplosis robiniae. Table S7. Akaike Information Criterion
(AIC) values for Parectopa robiniella. Table S8. Akaike Information
Criterion (AIC) values for Macrosaccus robiniella. Table S9. Akaike
Information Criterion (AIC) values for Obolodiplosis
robiniae.
Copyright notice: This dataset is made available under the Open
Database License (http://opendatacommons.org/licenses/odbl/1.0/).
The Open Database License (ODbL) is a license agreement intended to
allow users to freely share, modify, and use this Dataset while
maintaining this same freedom for others, provided that the
original source and author(s) are credited.
Link: https://doi.org/10.3897/neobiota.69.71949.suppl2
Abstract
Introduction
Methods
Results
Discussion
Conclusion
Acknowledgements
References